Fast Sequences of Non-spatial State Representations in Humans

Neuron

Volumn 91, Issue 1, 2016, Pages 194-204

  Kurth Nelson, Zeb ^a   Economides, Marcos ^a   Dolan, Raymond J ^a   Dayan, Peter ^b  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ARTICLE; BRAIN FUNCTION; CLASSIFIER; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN EXPERIMENT; LEARNING; MAGNETOENCEPHALOGRAPHY; MALE; MENTAL TASK; NEURAL REPRESENTATION; NON INVASIVE MEASUREMENT; PLANNING; PRIORITY JOURNAL; TASK PERFORMANCE; ADOLESCENT; BRAIN; PHYSIOLOGY; PROCEDURES; VISION; VISUAL CORTEX; YOUNG ADULT;

ADOLESCENT; ADULT; BRAIN; FEMALE; HUMANS; LEARNING; MAGNETOENCEPHALOGRAPHY; MALE; TASK PERFORMANCE AND ANALYSIS; VISUAL CORTEX; VISUAL PERCEPTION; YOUNG ADULT;

EID: 84991274127     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2016.05.028     Document Type: Article

References (72)

1. Allen, T.A., Salz, D.M., McKenzie, S., Fortin, N.J., Nonspatial Sequence Coding in CA1 Neurons. J. Neurosci. 36 (2016), 1547–1563.
2. Buckner, R.L., Carroll, D.C., Self-projection and the brain. Trends Cogn. Sci. 11 (2007), 49–57.
3. Buzsáki, G., Moser, E.I., Memory, navigation and theta rhythm in the hippocampal-entorhinal system. Nat. Neurosci. 16 (2013), 130–138.
4. Carr, M.F., Jadhav, S.P., Frank, L.M., Hippocampal replay in the awake state: a potential substrate for memory consolidation and retrieval. Nat. Neurosci. 14 (2011), 147–153.
5. Cheng, S., Frank, L.M., New experiences enhance coordinated neural activity in the hippocampus. Neuron 57 (2008), 303–313.
6. Collin, S.H.P., Milivojevic, B., Doeller, C.F., Memory hierarchies map onto the hippocampal long axis in humans. Nat. Neurosci. 18 (2015), 1562–1564.
7. Cornwell, B.R., Johnson, L.L., Holroyd, T., Carver, F.W., Grillon, C., Human hippocampal and parahippocampal theta during goal-directed spatial navigation predicts performance on a virtual Morris water maze. J. Neurosci. 28 (2008), 5983–5990.
8. Dalal, S., Jerbi, K., Bertrand, O., Adam, C., Ducorps, A., Schwartz, D., Martinerie, J., Lachaux, J.-P., Simultaneous MEG-intracranial EEG: new insights into the ability of MEG to capture oscillatory modulations in the neocortex and the hippocampus. Epilepsy Behav. 28 (2013), 288–292.
9. Danker, J.F., Anderson, J.R., The ghosts of brain states past: remembering reactivates the brain regions engaged during encoding. Psychol. Bull. 136 (2010), 87–102.
10. Davidson, T.J., Kloosterman, F., Wilson, M.A., Hippocampal replay of extended experience. Neuron 63 (2009), 497–507.
11. Diba, K., Buzsáki, G., Forward and reverse hippocampal place-cell sequences during ripples. Nat. Neurosci. 10 (2007), 1241–1242.
12. Dragoi, G., Tonegawa, S., Preplay of future place cell sequences by hippocampal cellular assemblies. Nature 469 (2011), 397–401.
13. Eichenbaum, H., Cohen, N.J., Can we reconcile the declarative memory and spatial navigation views on hippocampal function?. Neuron 83 (2014), 764–770.
14. Eschenko, O., Ramadan, W., Mölle, M., Born, J., Sara, S.J., Sustained increase in hippocampal sharp-wave ripple activity during slow-wave sleep after learning. Learn. Mem. 15 (2008), 222–228.
15. Euston, D.R., Tatsuno, M., McNaughton, B.L., Fast-forward playback of recent memory sequences in prefrontal cortex during sleep. Science 318 (2007), 1147–1150.
16. Foster, D.J., Wilson, M.A., Reverse replay of behavioural sequences in hippocampal place cells during the awake state. Nature 440 (2006), 680–683.
17. Foster, D.J., Wilson, M.A., Hippocampal theta sequences. Hippocampus 17 (2007), 1093–1099.
18. Girardeau, G., Benchenane, K., Wiener, S.I., Buzsáki, G., Zugaro, M.B., Selective suppression of hippocampal ripples impairs spatial memory. Nat. Neurosci. 12 (2009), 1222–1223.
19. Guitart-Masip, M., Barnes, G.R., Horner, A., Bauer, M., Dolan, R.J., Duzel, E., Synchronization of medial temporal lobe and prefrontal rhythms in human decision making. J. Neurosci. 33 (2013), 442–451.
20. Gupta, A.S., van der Meer, M.A.A., Touretzky, D.S., Redish, A.D., Hippocampal replay is not a simple function of experience. Neuron 65 (2010), 695–705.
21. Gupta, A.S., van der Meer, M.A.A., Touretzky, D.S., Redish, A.D., Segmentation of spatial experience by hippocampal θ sequences. Nat. Neurosci. 15 (2012), 1032–1039.
22. Hämäläinen, M., Hari, R., Ilmoniemi, R.J., Knuutila, J., Lounasmaa, O.V., Magnetoencephalography–theory, instrumentation, and applications to noninvasive studies of the working human brain. Rev. Mod. Phys. 65 (1993), 413–497.
23. Hoffman, K.L., McNaughton, B.L., Coordinated reactivation of distributed memory traces in primate neocortex. Science 297 (2002), 2070–2073.
24. Huys, Q.J., Eshel, N., O'Nions, E., Sheridan, L., Dayan, P., Roiser, J.P., Bonsai trees in your head: how the pavlovian system sculpts goal-directed choices by pruning decision trees. PLoS Comput. Biol., 8, 2012, e1002410.
25. Huys, Q.J., Lally, N., Faulkner, P., Eshel, N., Seifritz, E., Gershman, S.J., Dayan, P., Roiser, J.P., Interplay of approximate planning strategies. Proc. Natl. Acad. Sci. USA 112 (2015), 3098–3103.
26. Jadhav, S.P., Kemere, C., German, P.W., Frank, L.M., Awake hippocampal sharp-wave ripples support spatial memory. Science 336 (2012), 1454–1458.
27. Jensen, O., Lisman, J.E., Hippocampal sequence-encoding driven by a cortical multi-item working memory buffer. Trends Neurosci. 28 (2005), 67–72.
28. Ji, D., Wilson, M.A., Coordinated memory replay in the visual cortex and hippocampus during sleep. Nat. Neurosci. 10 (2007), 100–107.
29. Johnson, A., Redish, A.D., Neural ensembles in CA3 transiently encode paths forward of the animal at a decision point. J. Neurosci. 27 (2007), 12176–12189.
30. Káli, S., Dayan, P., Off-line replay maintains declarative memories in a model of hippocampal-neocortical interactions. Nat. Neurosci. 7 (2004), 286–294.
31. Karlsson, M.P., Frank, L.M., Awake replay of remote experiences in the hippocampus. Nat. Neurosci. 12 (2009), 913–918.
32. Killian, N.J., Jutras, M.J., Buffalo, E.A., A map of visual space in the primate entorhinal cortex. Nature 491 (2012), 761–764.
33. Kuhl, B.A., Chun, M.M., Successful remembering elicits event-specific activity patterns in lateral parietal cortex. J. Neurosci. 34 (2014), 8051–8060.
34. Kurth-Nelson, Z., Barnes, G., Sejdinovic, D., Dolan, R., Dayan, P., Temporal structure in associative retrieval. eLife, 4, 2015, e04919.
35. Lansink, C.S., Goltstein, P.M., Lankelma, J.V., McNaughton, B.L., Pennartz, C.M.A., Hippocampus leads ventral striatum in replay of place-reward information. PLoS Biol., 7, 2009, e1000173.
36. LaValle, S.M., Planning Algorithms. 2006, Cambridge University Press, Cambridge, New York.
37. Lee, A.K., Wilson, M.A., Memory of sequential experience in the hippocampus during slow wave sleep. Neuron 36 (2002), 1183–1194.
38. Louie, K., Wilson, M.A., Temporally structured replay of awake hippocampal ensemble activity during rapid eye movement sleep. Neuron 29 (2001), 145–156.
39. Milivojevic, B., Doeller, C.F., Mnemonic networks in the hippocampal formation: from spatial maps to temporal and conceptual codes. J. Exp. Psychol. Gen. 142 (2013), 1231–1241.
40. Mnih, V., Kavukcuoglu, K., Silver, D., Rusu, A.A., Veness, J., Bellemare, M.G., Graves, A., Riedmiller, M., Fidjeland, A.K., Ostrovski, G., et al. Human-level control through deep reinforcement learning. Nature 518 (2015), 529–533.
41. Muller, R.U., Stead, M., Pach, J., The hippocampus as a cognitive graph. J. Gen. Physiol. 107 (1996), 663–694.
42. Nádasdy, Z., Hirase, H., Czurkó, A., Csicsvari, J., Buzsáki, G., Replay and time compression of recurring spike sequences in the hippocampus. J. Neurosci. 19 (1999), 9497–9507.
43. Nyberg, L., Habib, R., McIntosh, A.R., Tulving, E., Reactivation of encoding-related brain activity during memory retrieval. Proc. Natl. Acad. Sci. USA 97 (2000), 11120–11124.
44. O'Keefe, J., Nadel, L., The hippocampus as a cognitive map. 1978, Oxford University Press.
45. Ólafsdóttir, H.F., Barry, C., Saleem, A.B., Hassabis, D., Spiers, H.J., Hippocampal place cells construct reward related sequences through unexplored space. eLife, 4, 2015, e06063.
46. Pezzulo, G., van der Meer, M.A.A., Lansink, C.S., Pennartz, C.M.A., Internally generated sequences in learning and executing goal-directed behavior. Trends Cogn. Sci. 18 (2014), 647–657.
47. Pfeiffer, B.E., Foster, D.J., Hippocampal place-cell sequences depict future paths to remembered goals. Nature 497 (2013), 74–79.
48. Polyn, S.M., Natu, V.S., Cohen, J.D., Norman, K.A., Category-specific cortical activity precedes retrieval during memory search. Science 310 (2005), 1963–1966.
49. Redish, A.D., Beyond the Cognitive Map. 1999, MIT Press.
50. Riggs, L., Moses, S.N., Bardouille, T., Herdman, A.T., Ross, B., Ryan, J.D., A complementary analytic approach to examining medial temporal lobe sources using magnetoencephalography. Neuroimage 45 (2009), 627–642.
51. Schapiro, A.C., Kustner, L.V., Turk-Browne, N.B., Shaping of object representations in the human medial temporal lobe based on temporal regularities. Curr. Biol. 22 (2012), 1622–1627.
52. Schmidt, B., Redish, A.D., Neuroscience: Navigation with a cognitive map. Nature 497 (2013), 42–43.
53. Shapiro, M.L., Eichenbaum, H., Hippocampus as a memory map: synaptic plasticity and memory encoding by hippocampal neurons. Hippocampus 9 (1999), 365–384.
54. Shohamy, D., Daw, N.D., Integrating memories to guide decisions. Curr. Opin. Behav. Sci. 5 (2015), 85–90.
55. Siapas, A.G., Wilson, M.A., Coordinated interactions between hippocampal ripples and cortical spindles during slow-wave sleep. Neuron 21 (1998), 1123–1128.
56. Sirota, A., Csicsvari, J., Buhl, D., Buzsáki, G., Communication between neocortex and hippocampus during sleep in rodents. Proc. Natl. Acad. Sci. USA 100 (2003), 2065–2069.
57. Skaggs, W.E., McNaughton, B.L., Replay of neuronal firing sequences in rat hippocampus during sleep following spatial experience. Science 271 (1996), 1870–1873.
58. Skaggs, W.E., McNaughton, B.L., Wilson, M.A., Barnes, C.A., Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus 6 (1996), 149–172.
59. Stephen, J.M., Ranken, D.M., Aine, C.J., Weisend, M.P., Shih, J.J., Differentiability of simulated MEG hippocampal, medial temporal and neocortical temporal epileptic spike activity. J. Clin. Neurophysiol. 22 (2005), 388–401.
60. Sutton, R.S., Dyna, an Integrated Architecture for Learning. 1991, Planning, and Reacting.
61. Takahashi, S., Hierarchical organization of context in the hippocampal episodic code. eLife, 2, 2013, e00321.
62. Takahashi, S., Episodic-like memory trace in awake replay of hippocampal place cell activity sequences. eLife, 4, 2015, e08105.
63. Tanaka, K.Z., Pevzner, A., Hamidi, A.B., Nakazawa, Y., Graham, J., Wiltgen, B.J., Cortical representations are reinstated by the hippocampus during memory retrieval. Neuron 84 (2014), 347–354.
64. Tavares, R.M., Mendelsohn, A., Grossman, Y., Williams, C.H., Shapiro, M., Trope, Y., Schiller, D., A Map for Social Navigation in the Human Brain. Neuron 87 (2015), 231–243.
65. Tolman, E.C., Cognitive maps in rats and men. Psychol. Rev. 55 (1948), 189–208.
66. van der Meer, M.A.A., Redish, A.D., Covert Expectation-of-Reward in Rat Ventral Striatum at Decision Points. Front. Integr. Nuerosci., 3, 2009, 1.
67. van der Meer, M.A.A., Johnson, A., Schmitzer-Torbert, N.C., Redish, A.D., Triple dissociation of information processing in dorsal striatum, ventral striatum, and hippocampus on a learned spatial decision task. Neuron 67 (2010), 25–32.
68. van der Meer, M., Kurth-Nelson, Z., Redish, A.D., Information processing in decision-making systems. Neuroscientist 18 (2012), 342–359.
69. Wierzynski, C.M., Lubenov, E.V., Gu, M., Siapas, A.G., State-dependent spike-timing relationships between hippocampal and prefrontal circuits during sleep. Neuron 61 (2009), 587–596.
70. Wikenheiser, A.M., Redish, A.D., The balance of forward and backward hippocampal sequences shifts across behavioral states. Hippocampus 23 (2013), 22–29.
71. Wikenheiser, A.M., Redish, A.D., Hippocampal theta sequences reflect current goals. Nat. Neurosci. 18 (2015), 289–294.
72. Wimmer, G.E., Shohamy, D., Preference by association: how memory mechanisms in the hippocampus bias decisions. Science 338 (2012), 270–273.